Double labeling of GABA and cytochrome oxidase in the macaque visual cortex: Quantitative EM analysis

Abstract

In the primate striate cortex, cytochrome oxidase (CO)-rich puffs differ from CO-poor interpuffs in their metabolic levels and physiological properties. The neurochemical basis for their metabolic and physiological differences is not well understood. The goal of the present study was to examine the relationship between the distribution of gamma aminobutyric acid (GABA)/non-GABA synapses and CO levels in postsynaptic neuronal profiles and to determine whether or not a difference existed between puffs and interpuffs. By combining CO histochemistry and postembedding GABA immunocytochemistry on the same ultrathin sections, the simultaneous distribution of the two markers in individual neuronal profiles was quantitatively analyzed. In both puffs and interpuffs, GABA-immunoreactive (GABA-IR) neurons were the only cell type that received both non-GABA-IR (presumed excitatory) and GABA-IR (presumed inhibitory) axosomatic synapses, and they had three times as many mitochondria darkly reactive for CO than non-GABA-IR neurons, which received only GABA-IR axosomatic synapses. GABA-IR neurons and terminals in puffs had a larger mean size, about twice as many darkly reactive mitochondria, and a higher ratio of non-GABA-IR to GABA-IR axosomatic synapses than those in interpuffs (2.3:1 vs. 1.6:1; P < 0.01). There were significantly more synapses of both non-GABA-IR and GABA-IR types in the neuropil of puffs than of interpuffs; however, the ratio of non-GABA-IR to GABA-IR synapses was significantly higher in puffs (2.86:1) than in interpuffs (2.08:1; P < 0.01). Our results are consistent with the hypothesis that the level of oxidative metabolism in postsynaptic neurons and neuronal processes is tightly governed by the strength and proportion of excitatory over inhibitory synapses. Thus, the present results suggest that (1) GABA-IR neurons in the macaque striate cortex have a higher level of oxidative metabolism than non-GABA ones because their somata receive direct excitatory synapses and their terminals are more tonically active; (2) the higher proportion of presumed excitatory synapses in puffs imposes a greater energy demand there than in interpuffs; and (3) excitatory synaptic activity may be more prominent in puffs than in interpuffs because puffs receive a greater proportion of excitatory synapses from multiple sources including the lateral geniculate nucleus, which is not known to project to the interpuffs.

Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex

“…This finding is in agreement with previous data in vivo showing that, compared with excitatory neurons, putative inhibitory neurons respond more vigorously, at lower thresholds, and with shorter latencies (Simons, 1978;Yamamoto et al, 1988;Simons and Carvell, 1989;Swadlow, 1989;Welker et al, 1993) and are metabolically more active (Nie and Wong-Riley, 1995;McCasland and Hibbard, 1997). It was previously suggested (Simons, 1995) that the thalamocortical synapses may be more effective on inhibitory neurons because they impinge on their Figure 6.…”

GABAergic Neurons in Barrel Cortex Show Strong, Whisker-Dependent Metabolic Activation during Normal Behavior

“…We also show that the relative levels of activation in excitatory and inhibitory neurons vary systematically by cortical lamina. Our data are consistent with hypotheses based on limited available samples from single-unit recordings from barrels, from the CO data of Wong-Riley et al (1989, 1994Nie and Wong-Riley, 1995) and from electron microscopic studies of synaptic distributions in barrel circuits (White, 1989).…”

“…With respect to our findings, the most definitive of these is an ultrastructural double-labeling study for CO and GABA (Nie and Wong-Riley, 1995) in macaque striate cortex. Their data show that GABAergic type C neurons receive both excitatory and inhibitory axosomatic synapses and contain darkly CO-reactive mitochondria, whereas non-GABA neurons receive only GABAergic axosomatic synapses and have lightly CO-reactive mitochondria.…”

“…Wong-Riley and colleagues , 1994Nie and Wong-Riley, 1995) have shown that GABAergic type C cells in striate cortex of monkeys contain mitochondria that are darkly CO-reactive. However, CO represents a relatively long-term measure (hours or days) of oxidative metabolism (Wong-Riley and Welt, 1980;Wong-Riley and Carroll, 1984;Deyoe et al, 1995).…”

Highly Energized Inhibitory Interneurons are a Central Element for Information Processing in Cortical Networks

“…74,121 Similar observations have been made in interneuron subpopulations of the visual cortex. 124,125 We note that these findings High energy utilization 41,57,63,64,67 Exquisite sensitivity to metabolic stress 41,44,47,163,164 AP, action potential. Some unique features of (A) fast-spiking, parvalbuminpositive interneurons and (B) gamma oscillations (30 to 100 Hz) are summarized, including a selection of key references.…”